Anti-Escherichia coli Activity of Herbal Medicines: A Systematic Literature Review

authors:

avatar Khadijeh Saravani 1 , * , avatar Fardin Ali Malayeri 2

Assistant Professor of Forensic Medicine and Toxicology, Faculity of Medicine, Zabol University of Medical Sciences, Zabol, Iran
Department of clinical biochemistry, Faculity of Medicine, Zabol University of Medical Sciences, Zabol, Iran

how to cite: Saravani K, Malayeri F A. Anti-Escherichia coli Activity of Herbal Medicines: A Systematic Literature Review. Gene Cell Tissue. 2020;7(4):e96241. https://doi.org/10.5812/gct.96241.

Abstract

Context:

Infectious diseases are the cause of death worldwide. As antibiotic resistance is rising, researchers are looking for new therapies. The Gram-negative bacterium Escherichia coli, causes acquired hospital infections and results in intestinal infections and many infections out of the intestine, like urinary tract infections (UTI), cholecystitis, wound infections, meningitis, septicemia, pulmonary infections, etc. Plants are a good source of bioactive compounds; hence, they can be effective in treating several illnesses. The purpose of this research was to peruse the antibacterial activity of various herbal extracts on E. coli.

Evidence Acquisition:

This research was obtained from various articles published from 2000 to 2017 from the PubMed, ScienceDirect, Springer, Islamic Science Citation, and Magiran databases. The keywords used were E. coli, herbs, natural antibiotics, and antimicrobial activity.

Results:

The results showed that the ethanolic extracts of medicinal plants showed better inhibitory function against E. coli than other solvents.

Conclusions:

The obtained results showed that medicinal herbs can be considered as the main medicinal agents capable of affecting infections caused by E. coli.

1. Context

The use of herbal medicinal compounds has long been considered by a human being. The drugs that are used widely worldwide to cure several diseases, including bacterial, viral, and fungal infections, and all kinds of metabolic diseases, even cancer, are naturally occurring compounds (1-3). The herbal medicines containing herbal compounds and their derivatives account for about one-third of the total available drugs (4, 5). One of the main reasons for the desire of the medical community to use herbal compounds is their low side effect compared with chemical drugs, which has been proved during many years in traditional medicine (6, 7). In addition, the use of industrial medicines and chemical compounds can lead to undesirable metabolic reactions, and, in most cases, free radicals and peroxides are produced. Herbal medicines are rich in various bioactive compounds that prevent the production of oxidants (8).

Enterohemorrhagic Escherichia coli is one of six types of E. coli recognized as the cause of diarrhea. It provides cytotoxins, such as verocytotoxin or Shiga-like toxin, which causes hemorrhagic colitis. This organism was first identified as a cause of illness in 1982, and its related diseases have been increased. E. coli has recently been widely considered as it is easily transferred by human and animal waste and contaminates the environment (9, 10).

E. coli is an opportunistic pathogen that is frequently colonized in the human colonic region (11). At the equal opportunity, it is one of the most prevalent causative agents for the urinary tract injury (UTI) and abdominal diseases. The most important virulence part of microorganisms, especially Gram-negative bacteria, is adhesion to the host cell receptors. This adhesion is caused by particular adhesins, which are surrounded in fimbriae, e.g., pili (pilus adhesion) in Gram-negative bacteria and are on the cell wall (non-pilus adhesion) in Gram-positive bacteria.

E. coli can acquire antimicrobial resistance mechanisms, such as encoding the genes of the enzymes, such as β-lactamases, the genes that alter the bacterial cell wall, which results in no binding site for antimicrobial agent and condensation of outlet pumps, translation, and transduction (12). Efflux pumps are transportation proteins involved in the extrusion of toxic substrates (including nearly all types of clinically important antibiotics) (13). Efflux pumps can be discriminated from multidrug efflux pumps, and the extrusion of antimicrobial agents via these efflux pumps is a major factor in antimicrobial resistance (14). Cells can use proton-driven antiporters and/or ATP-driven transporters (ATP-binding cassette) to expel medicines (15). Efflux pump inhibitors can be utilized to reduce the efflux of antibiotics from bacterial cells, suggesting that antibiotics, such as ciprofloxacin can be used to restore medicinal protection. Verapamil and MC-207,110 are common utilized efflux pump inhibitors (15). As a consequence of antibiotic defense, new antimicrobials that will be restored or used with antibiotics are needed.

2. Evidence Acquisition

Studies in English published from 2000 to 2017 were searched using Web of Science, PubMed, Scopus, Google Scholar, and ScienceDirect using the keywords Escherichia coli, Plant extracts, herbal plants, herbal medicines, and antibacterial activity. Further citations were recognized by evaluating the reference lists of related articles.

3. Results

The reported minimum inhibitory concentration (MIC) values of the used plants against E. coli are summarized in Table 1. As can be found, the majority of the studied plants had bacteriostatic activity, and some had both bacteriostatic and as well as bactericidal activity.

Table 1.

In Vitro Activity of the Medicinal Plants Affecting Escherichia coli

Scientific NameFamily NamePart UsedResultRef
Stachys inflata BenthLamiaceaeAerial partsThe inhibition zone diameter of methanol extract of this plant was 11 mm, and the MIC of methanol extract was 500 mg/ml, and MIC of a-Terpineol and Linalool were 500 and 125 mg/mL, respectively. (16)
Heracleum lasiopetalum BoissApiaceaeFruitAntibacterial activity of ethanol extract and essential oil were 18 and 17 mm, respectively. MIC of the ethanol extract and essential oil were 156.25 and 39 µg/mL, respectively. (17)
Ziziphora teniur L.LamiaceaeLeavesThe antibacterial activity of the ethanol extract was 18 mm using agar diffusion assay (100 µg/disc). MIC of the ethanol extract was 625 μg/mL.(17, 18)
Euphorbia helioscopa L.EuphorbiaceaeAerial PartsIn each plate, one positive control (gentamycin 0.8 mg/0.2 mL and one negative control (methanol 0.2 mL) were included. Zones of inhibition were measured, and antimicrobial activities of the extracts were measured.(19)
Euphorbia microsciadia BoissEuphorbiaceaeAerial PartsIn each plate, one positive control (gentamycin 0.8 mg/0.2 mL and one negative control (methanol 0.2 ml) were included. (19)
Centaurea cyanus LAsteraceaeTotal partsIn each plate, one positive control (gentamycin 0.8 mg/0.2 mL and one negative control (methanol 0.2 ml) were included. (19)
Verbascum speciosum SchradScrophulariaceaeLeavesIn each plate, one positive control (gentamycin 0.8 mg/0.2 mL and one negative control (methanol 0.2 ml) were included. (19)
Apium graveolensApiaceaeLeavesInhibition zone diameter was 7-9 mm using agar well-diffusion bioassay (2 mg/well).(20)
Trigonella foenum-graecumLeguminosaepapilionoideaeSeedsInhibition zone diameter was >15mm using agar well-diffusion bioassay (2 mg/well).(20)
Ziziphus ziziphusRhamnaceaeFruitInhibition zone diameter was 10-14 mm using agar well diffusion bioassay (2 mg/well).(18, 20, 21)
Rhus coriariaAnacardiaceaeFruitAntibacterial activity of the ethanolic extracts using the disc and well diffusion assays was 17 and 24 mm, respectively. The zone of inhibition was 17 mm through disc diffusion assay. MIC of extracts was 0.20%.(22)
Funmaria vaillantiiFumariaceaeFlowers and stemsThe zone of inhibition using the agar diffusion test was 11 mm and MIC was 125 µg/mL.(23)
Quercus brantiiFagaceaeFruitThe inhibition zone diameter was 12 mm.(24)
Artemisia siberiAsteraceaeAerial partsThe diameter of the inhibitory zone diameter was 12 mm.(25)
Wasabia japonicaBrassicaceaeTotal partThe results indicated that the MIC of wasabi against E. coli O157:H7 and S. aureus was 1% (equal to 10 mg/mL) and 4%, respectively.(26)
PeganumharmalaNitrariaceaeFruitMIC was 5 mg/mL.(27)
PeganumharmalaNitrariaceaeRootMIC was 0.625 mg/mL.(27, 28)
Allium sativumAmaryllidaceaeFruitThe inhibition zone diameter around the discs varied from 17 - 35 mm, indicating that all 13 AmpC positive isolates (100%) were sensitive to garlic extract. One out of 13 E. coli sequesters had a MIC of 2.5 mg/ml for alcoholic distillate of A. sativum. The highest MIC and MBC values of the alcoholic distillate of A. sativum were 5 mg/ml and 10 mg/mL, respectively. The highest and lowest MIC of AmpC positive E. coli isolates were determined to be > 256 and 16 µg/mL, respectively.(29)
Trachyspermum ammiApiaceaeSeedThe highest MIC of the needful oil was 100 ppm against E. coli.(18, 30, 31)
Hibiscus sabdariffalMalvaceaeFlowerThe highest MIC value was detected to be 20 mg/mL against two E. coli isolates.(32)
Cassia auriculataFabaceaeLeavesThe MIC and MBC of ethyl acetate extract of the leaves and flowers were measured. The highest MIC was 50 - 125 mg/mL.(33)
ArtichokeAsteraceaeLeavesThe results showed that the inhibition zone diameter of the ethanolic, methanolic, and estrogenic extracts of leaves was 11 mm, while for the ethanolic and methanol extracts of the stem, this rate was equal to 8 - 14 and 11 mm, respectively(34)
Punica granatumLythraceaePeelThe PIC of the ethanol extract prepared from peel was 14.2 ± 0.61(35)
Zataria multifloraLamiaceaeLeavesThe correlation coefficient of the concentration of essential oil of Z. multiflora with the logarithm of the bacteria was studied at temperatures of 4, and 10°C and the results were 0.701 and 0.599, indicating that by increasing the essential oil concentration, the growth rate of the bacteria during the storage period is reduced and efficacy of the necessary oil on the growth of bacteria is significant.(36)
HoneyThe results showed that the inhibitory zone diameter of honey, licorice, honey, apples, and honey are 1 ± 13, 5/0 ± 12, and 5/0 ± 9 mm(37)
RoseRosalesLeavesThe inhibitory zone diameter of the ethanolic extract of rose was 14 mm, and its MIC was 25 mg.(38, 39)
Aloe veraAsphodelaceaeLeaves MIC was 50 µg.(39)
Fennel Bakhtiari--MIC and MBC of alcoholic extract of Bakhtiari fennel against E. coli were 3.12 mg/ml and zero, respectively.(40)
Peganum harmalaNitrariaceaeLeaves Compared with the controls, there was no significant difference n the efficacy of the P. harmala juice on microbial growth.(41, 42)
Eucalyptus globulusMyrtaceaeLeavesThe results indicated that essential oil of the leaves of E. globulus has an antibacterial effect against E. coli and S. aureus.(41, 42)
Cyminum cuminumApiaceaeSeedEthanol extract of seeds showed antimicrobial activity against the E. coli biofilm.(31, 43)
Zataria multifloraLamiaceaeLeavesThe extract represented inhibitory activity against E. coli.(44)
Coccinia grandisCucurbitaceaeLeavesAqueous, acetone, and ethanol extracts of the leaves of C. grandis were examined for antibacterial effect using the agar well diffusion method. Ethanol extract of the leaves displayed antibacterial effect against biofilm producing strains UPEC 17 and 82, whereas the aqueous and acetone extracts displayed antimicrobial effect only against UPEC 57. Ethanol extract of levees showed inhibitory action against ESBL producing UPEC 87 and 96, while the aqueous extract inhibited the growth of only UPEC 85.(45, 46)
Avicenna MarinaAcanthaceae-The glycerol extract of Avicenna Marina showed inhibitory activity against E. coli and P. digitatum.(45, 46)
Calotropis proceraApocynaceaeLeave The results illustrated that a total of 30 of 80 (37.5%) isolates harbored ESBL enzymes.(47)
Punica granatum‎LythraceaeLeaveMIC of Punica granatum was 4.0mg/ml, which showed a good antibacterial activity against Shiga toxin produced by E. coli.(48)
Punica granatum‎LythraceaeLeaveMIC was 0.49 to 1.95 mg/ml and MBC was 1.95 to 3.91 mg/ml.(49)
Punica granatumPomegranateLeaveIn this study, six extracts were prepared from the powdered leaves of P. granatum. The MIC was found to be from 0.5 to 20.07%. The highest MIC was obtained using the aqueous extract and the lowest was related to the ethyl acetate extract.(50)
Ocimum gratissimumLamiaceaeThe MIC presented by Ocimum gratissimum against the E. coli strains was 20,000 μg/mL.(51)
Butea monospermaFabaceaeFlowerThe extract exhibited antibacterial activity against E. coli and S. aureus.(52)
Physalis pubescensSolanaceaeLeavesThe extracts exhibited the highest inhibitory diameter zone of 12.5 to 13.6 mm.(53)
Ruellia tuberosa L.AcanthaceaeRootThe inhibitory diameter zone against E. coli, was 7, 7, 7, 10.75, 11.00, and 15.00 mm for the concentrations of 5, 10, 20, 50, 75, and 100% (v/v), respectively.(54)
Rubia cordifoliaRubiaceaeRootThe plant could be a potential candidate for an alternative antibacterial agent to combat the invasion of drug-resistant organisms.(55)

4. Discussion

Several studies have revealed that herbal medicines are good sources of compounds with antioxidant and antimicrobial activity, which are able to protect the body against cellular oxidation and pathogens. Therefore, the classification of various herbal medicines because of their antioxidant and antimicrobial potentials is considerable. Herbal drugs that are safe and protect against pathogens are beneficial candidates for generating new antimicrobial medicines and have been long used in many cultures.

The main medicinal plants and their major compounds that can affect E. coli are as follows: Allicin (S-(2-propenyl) 2-propene-1-sulfinothioate) is the most biologically active sulfur-containing compound of garlic (A. sativum) (56), thymol, γ-terpinene, para-cymene, and α- and β-pinene are the most biologically active sulfur-containing compounds of Trachyspermum ammi), the major compounds identified in the essential oil of Hibiscus sabdariffal are hexadecanoic acid and linoleic acid; Carvacrol and Thymol are the most frequent compounds of the Zataria multiflora Z (57); linalool and β-pinene are the most biologically active sulfur-containing compound of Aloe vera and Teucrium polium (58); in Eucalyptus globulus, 1,8-cineole, globulol, trans-pinocarveol, and alpha-terpineol are the main components (59); Cuminaldehyde, p-cymene, β-pinene, α-terpinen-7-al, γ-terpinene, p-cymen-7-ol, and thymol are found in Cyminum cuminum (60), n-tetracosane, n-eicosane, tetratriacotane, 7-octadecanal , and tricosane are the major constituents in Coccinia grandis (61), (the major compounds in the leaf essential oil of Laportia ovalifolia and Spondias mombin are δ-cadinene, α-humulene, γ-muurolene, α-gurjunene, α-muurolene, 5-isocedranol, and δ-cadinene) (62), in Ficus exasperate, the significant compounds are 1,8-cineole, (Ε)-phytol, and p-cymene) (63), and sesquiterpene β-caryophyllene (flower: 15.2%, stem: 8.1%) are highly found in Ageratum conyzoides; six of the identified compounds, including β-copaene, hexanal, trans-cadina-1(6),4-diene, α-calacorene, caryophylla-4(12),8(13)-diene-5-β-ol, and 1,10-di-epi-cubenol are reported for the first time as constituents of A. conyzoides) (64); the main chemical constituents in Punica granatum peel seeds were propanoic acid, benzenedicarboxylic acid, methoxypropionic acid, and methylamine (65), regarding Quercus Infectoria, both phenolic and flavonoid compounds are found in the methanol extract; however, phenolic compounds are more than the flavonoid compounds (66); phenolic compounds, flavonoids, saponins, steroids, tannins, xanthoproteins, carboxylic acids, coumarins, and carbohydrates were detected in the methanol extract of Peltophorum pterocarpum flowers (67); in P. granatum, Cissus welwitschii, Triumfetta welwitschii, Entada Africana (bark), Lannae acida (stem bark), and Terminalia avicennoides, bioactive hydrolysable tannin compounds, including ellagic acid, punicalagin, flavogallonic acid, and terchebulin) (68) are highly available; four flavonoids, such as 6,7-(2”,2”-dimethyl chromeno)-8-γ,γ-dimethyl allyl flavanone, 3’,4’dihydroxy-7,8 (2”,2”- dimethyl chromeno)-6-γ,γ dimethyl allyl flavonol, 7-methyltectorigenin, and Irisolidone were isolated from the leaves of Lannea acida) (69); α-pinene, E-β-ocimene, terpinolene, α-terpineol, eugenol, β-cubenene, β-caryophyllene, γ- muurolene, -muurolene, epi-cubebol, and -cubebol, and δ-cadinene in less quantity were detected in Ocimum gratissimum (70); and new anthraquinones, namely 1-hydroxy-2,7-dimethyl anthraquinone, 2-hydroxy -6-methyl anthraquinone, 2,6-dihydroxy anthraquinone, 1-hydroxy 2-methyl anthraquinone, nordamnacanthal, physcion, 1,4-dihydroxy 6-methyl-anthraquinone, 1,4-dihydroxy 2-methyl anthraquinone, 1,5-dihydroxy 2-methyl anthraquinone, 3-prenyl methoxy 1,4-naphthoquinone, 1-hydroxy 2-methoxy anthraquinone, 1,4-dihydroxy 2-methyl 5-methoxy anthraquinone or 1,4-dihydroxy 2-methyl 8-methoxy anthraquinone, 1,3-dimethoxy 2-carboxy anthraquinone, and rubiadin were isolated from Rubia cordifolia roots) (71). Additional information about medicinal plants effective against E. coli are presented in Table 1.

5. Conclusions

The strains of E. coli have consistently been shown resistance to various antibiotics, which has increased their pathogenicity; thus, finding new strategies to treat infections caused by them is of great importance.

Acknowledgements

References

  • 1.

    Tchakam PD, Lunga PK, Kowa TK, Lonfouo AHN, Wabo HK, Tapondjou LA, et al. Antimicrobial and antioxidant activities of the extracts and compounds from the leaves of Psorospermum aurantiacum Engl. and Hypericum lanceolatum Lam. BMC Complementary Altern Med. 2012;12(1):136. [PubMed ID: 22916964]. https://doi.org/10.1186/1472-6882-12-136.

  • 2.

    Davari A, Solouki M, Fazeli-Nasab B. [Effects of jasmonic acid and titanium dioxide nanoparticles on process of changes of phytochemical and antioxidant in genotypes of Satureja hortensis]. Eco-Phytochem J Med Plants. 2018;5(4):1-20. Persian.

  • 3.

    Fazeli-Nasab B. Evaluation of Antibacterial Activities of Hydroalcoholic Extract of Saffron Petals on Some Bacterial Pathogens. J Med Bacteriol. 2019;8(5, 6):8-20.

  • 4.

    Safavi F, Ebrahimi P, Mighani H. In vitro antibacterial activity of root and aerial parts of Scrophularia striata Bioss on Escherichia coli, Staphylococcus aureus and Bacillus cereus. Armaghane Dnesh. 2013;18(8):603-14.

  • 5.

    Rezaei-Nasab M, Komeili G, Fazeli-Nasab B. Gastroprotective effects of aqueous and hydroalcholic extract of Scrophularia striata on ethanol-induced gastric ulcers in rats. Braz J Microbiol. 2017;9(5):84-93.

  • 6.

    Nascimento GG, Locatelli J, Freitas PC, Silva GL. Antibacterial activity of plant extracts and phytochemicals on antibiotic-resistant bacteria. Braz J Microbiol. 2000;31(4):247-56. https://doi.org/10.1590/S1517-83822000000400003.

  • 7.

    Saeidi S, Fazeli-Nasab B. Evaluation of antibacterial and antifungal activity of various extracts of the Rhazya stricta , Capparis spinosa , cretica Cressa. New Find Vet Microbiol. 2019;2(1):57-66.

  • 8.

    Abdel-Hady AA, El-Nahas H, El Nabarawy S, Abdel Raouf H. Evaluation of the Antioxidant Activity and the Acute Oral Toxicity of Three Plant Extracts on Albino Mice. Middle East J Appl Sci. 2014;4(2):207-16.

  • 9.

    Smith SI, Aboaba OO, Odeigha P, Shodipo K, Adeyeye JA, Ibrahim A, et al. Plasmid profile of Escherichia coli 0157: H7 from apparently healthy animals. Afr J Biotechnol. 2003;2(9):322-4. https://doi.org/10.5897/AJB2003.000-1066.

  • 10.

    Valizadeh M, Beigomi M, Fazeli-Nasab B. Antibacterial and Anti biofilm effects of ethanol and aceton leaf extract of Momordica charantia and Tecomella undulata against Acinetobacter baumannii. Int J Adv Biol Biomed Res. 2020;8(4):403-18. https://doi.org/10.33945/sami/ijabbr.2020.4.6.

  • 11.

    Keikhaie KR, Fazeli-Nasab B, Jahantigh HR, Hassanshahian M. Antibacterial Activity of Ethyl Acetate and Methanol Extracts of Securigera securidaca, Withania sominefra, Rosmarinus officinalis and Aloe vera Plants against Important Human Pathogens. J Med Bacteriol. 2018;7(1-2):13-21.

  • 12.

    Tenover FC. Mechanisms of antimicrobial resistance in bacteria. Am J Med. 2006;119(6 Suppl 1):S3-10. discussion S62-70. [PubMed ID: 16735149]. https://doi.org/10.1016/j.amjmed.2006.03.011.

  • 13.

    Lacmata ST, Kuete V, Dzoyem JP, Tankeo SB, Teke GN, Kuiate JR. Antibacterial activities of selected Cameroonian plants and their synergistic effects with antibiotics against bacteria expressing MDR phenotypes. Evidence-Based Complement Altern Med. 2012;8(4):403-18. [PubMed ID: 22474511]. [PubMed Central ID: PMC3304440]. https://doi.org/10.1155/2012/623723.

  • 14.

    Fiamegos YC, Kastritis PL, Exarchou V, Han H, Bonvin AM, Vervoort J, et al. Antimicrobial and efflux pump inhibitory activity of caffeoylquinic acids from Artemisia absinthium against gram-positive pathogenic bacteria. PLoS One. 2011;6(4). e18127. [PubMed ID: 21483731]. [PubMed Central ID: PMC3070693]. https://doi.org/10.1371/journal.pone.0018127.

  • 15.

    Borges-Walmsley MI, McKeegan KS, Walmsley AR. Structure and function of efflux pumps that confer resistance to drugs. Biochem J. 2003;376(Pt 2):313-38. [PubMed ID: 13678421]. [PubMed Central ID: PMC1223791]. https://doi.org/10.1042/BJ20020957.

  • 16.

    Ebrahimabadi AH, Ebrahimabadi EH, Djafari-Bidgoli Z, Jookar Kashi F, Mazoochi A, Batooli H. Composition and antioxidant and antimicrobial activity of the essential oil and extracts of Stachys inflata Benth from Iran. Food Chem. 2010;119(2):452-8. https://doi.org/10.1016/j.foodchem.2009.06.037.

  • 17.

    Ghasemi Pirbalouti A, Malekpoor F, Enteshari S, Yousefi M, Momtaz H, Hamedi B. Antibacterial activity of some folklore medicinal plants used by Bakhtiari tribal in Southwest Iran. Int J Biol. 2010;2(2). https://doi.org/10.5539/ijb.v2n2p55.

  • 18.

    Nasab-Fazeli B, Sirousmehr A, Mirzaei N, Solimani M. Evaluation of total phenolic, flavenoeid content and antioxidant activity of Leaf and Fruit in 14 different genotypes of Ziziphus mauritiana L. in south of Iran. Eco-Phytochem J Med Plants. 2017;4(4):1-4.

  • 19.

    Bazzaz BS, Haririzadeh G. Screening of Iranian Plants for Antimicrobial Activity. Pharmaceutical Biology. 2008;41(8):573-83. https://doi.org/10.1080/13880200390501488.

  • 20.

    Bonjar S. Evaluation of antibacterial properties of some medicinal plants used in Iran. J Ethnopharmacol. 2004;94(2-3):301-5. [PubMed ID: 15325735]. https://doi.org/10.1016/j.jep.2004.06.007.

  • 21.

    Fazeli-Nasab B, Mirzaei N. Evaluation of Total Phenol and Flavonoid Content in a Wide Range of Local and imported Plants. J Ilam Univ Med Sci. 2018;26(2):141-54. https://doi.org/10.29252/sjimu.26.2.141.

  • 22.

    Fazeli MR, Amin G, Ahmadian Attari MM, Ashtiani H, Jamalifar H, Samadi N. Antimicrobial activities of Iranian sumac and avishan-e shirazi (Zataria multiflora) against some food-borne bacteria. Food Control. 2007;18(6):646-9. https://doi.org/10.1016/j.foodcont.2006.03.002.

  • 23.

    Jaberian H, Piri K, Nazari J. Phytochemical composition and in vitro antimicrobial and antioxidant activities of some medicinal plants. Food Chem. 2013;136(1):237-44. [PubMed ID: 23017418]. https://doi.org/10.1016/j.foodchem.2012.07.084.

  • 24.

    Khosravi AD, Behzadi A. Evaluation of the antibacterial activity of the seed hull of Quercus brantii on some gram negative bacteria. Pak J Med Sci. 2006;22(4):429-32.

  • 25.

    Behmanesh B, Heshmati GA, Mazandarani M, Rezaei MB, Ahmadi AR, Ghaemi EO, et al. Chemical Composition and Antibacterial Activity from Essential Oil of Artemisia sieberi Besser subsp. Sieberi in North of Iran. Asian J Plant Sci. 2007;6(3):562-4. https://doi.org/10.3923/ajps.2007.562.564.

  • 26.

    Lu Z, Dockery CR, Crosby M, Chavarria K, Patterson B, Giedd M. Antibacterial Activities of Wasabi against Escherichia coli O157:H7 and Staphylococcus aureus. Front Microbiol. 2016;7:1403. [PubMed ID: 27708622]. [PubMed Central ID: PMC5030237]. https://doi.org/10.3389/fmicb.2016.01403.

  • 27.

    Eshaghi Najafabadi R, Mohammadi M, Yousefi M, Habibi Z. Chemical Composition and Antibacterial Activity of Essential Oils from Flowers, Seeds and Stems ofHeracleum rechingeri (Manden) from Iran. J Essent Oil Bearing Plants. 2011;14(6):746-50. https://doi.org/10.1080/0972060x.2011.10643998.

  • 28.

    Darabpour E, Poshtkouhian Bavi A, Motamedi H, Seyyed Nejad SM. Antibacterial activity of different parts of Peganum harmala L. growing in Iran against multi-drug resistant bacteria. EXCLI J. 2011;10:252-63. [PubMed ID: 29033706]. [PubMed Central ID: PMC5611620].

  • 29.

    Shayan S, Bokaeian M, Shahraki S, Saeidi S. Prevalence of AmpC and ESBL Producing E. coli and Antibacterial Effect of Allim sativum on Clinical Isolates Collected from Zahedan Hospitals. Zahedan J Res Med Sci. 2014;16(4):6-10.

  • 30.

    Hassanshahian M, Bayat Z, Saeidi S, Shiri Y. Antimicrobial activity of Trachyspermum ammi essential oil against human bacterial. Int J Adv Biol Biomed Res. 2014;2(1):18-24.

  • 31.

    Fazeli-Nasab B. The effect of explant, BAP and 2,4-D on callus induction of Trachyspermum ammi. Potravinarstvo. 2018;12(1). https://doi.org/10.5219/953.

  • 32.

    Bokaeian M, Sheikh M, Shahi Z, Saeidi S. Antimicrobial activity of Hibiscus sabdariffal extract against human pathogen. Int J Adv Biol Biomed Res. 2014.

  • 33.

    Thulasi G, Amsaveni V. Antibacterial activity of Cassia auriculata against ESBL producing E. coli from UTI patients. Int J Microbiol Res. 2012;3(1):24-9.

  • 34.

    Dhama K, Tiwari R, Chakrabort S, Saminathan M, Kumar A, Karthik K, et al. Evidence Based Antibacterial Potentials of Medicinal Plants and Herbs Countering Bacterial Pathogens Especially in the Era of Emerging Drug Resistance: An Integrated Update. Int J Pharmacol. 2014;10(1):1-43. https://doi.org/10.3923/ijp.2014.1.43.

  • 35.

    Mostafa AA, Al-Askar AA, Almaary KS, Dawoud TM, Sholkamy EN, Bakri MM. Antimicrobial activity of some plant extracts against bacterial strains causing food poisoning diseases. Saudi J Biol Sci. 2018;25(2):361-6. [PubMed ID: 29472791]. [PubMed Central ID: PMC5815983]. https://doi.org/10.1016/j.sjbs.2017.02.004.

  • 36.

    Avaei A, Mohamadi Sani A, Mahmoodzadeh Vaziri B. Chemical composition and antimicrobial effect of the essential oil of Zataria multiflora Boiss endemic in Khorasan-Iran. Asian Pac J Trop Dis. 2015;5(3):181-5. https://doi.org/10.1016/s2222-1808(14)60649-6.

  • 37.

    Meda A, Lamien CE, Romito M, Millogo J, Nacoulma OG. Determination of the total phenolic, flavonoid and proline contents in Burkina Fasan honey, as well as their radical scavenging activity. Food Chem. 2005;91(3):571-7. https://doi.org/10.1016/j.foodchem.2004.10.006.

  • 38.

    Halpern SL. Sources and consequences of seed size variation in Lupinus perennis (Fabaceae): adaptive and non-adaptive hypotheses. Am J Bot. 2005;92(2):205-13. [PubMed ID: 21652397]. https://doi.org/10.3732/ajb.92.2.205.

  • 39.

    Nemati Niko Z, Ghajarbeygi P, Mahmoudi R, Mousavi S, Mardani K. Inhibitory Effects of Aloe Vera Gel Aqueous Extract and L. casei Against E. coli in Yoghurt. J Biol Today's World. 2016;5(9). https://doi.org/10.15412/j.jbtw.01050901.

  • 40.

    Barzegar H, Alizadeh Behbahani B, Mehrnia MA. Quality retention and shelf life extension of fresh beef using Lepidium sativum seed mucilage-based edible coating containing Heracleum lasiopetalum essential oil: an experimental and modeling study. Food Sci Biotechnol. 2020;29(5):717-28. [PubMed ID: 32419970]. [PubMed Central ID: PMC7221043]. https://doi.org/10.1007/s10068-019-00715-4.

  • 41.

    Mashreghi M, Niknia S. The Effect of Peganum harmala and Teucrium polium Alcoholic Extracts on Growth of Escherichia coli O157. Jundishapur J Microbiol. 2012;5(3):511-5. https://doi.org/10.5812/jjm.3665.

  • 42.

    Bachir RG, Benali M. Antibacterial activity of the essential oils from the leaves of Eucalyptus globulus against Escherichia coli and Staphylococcus aureus. Asian Pac J Trop Biomed. 2012;2(9):739-42. [PubMed ID: 23570005]. [PubMed Central ID: PMC3609378]. https://doi.org/10.1016/S2221-1691(12)60220-2.

  • 43.

    Bameri Z, Amini-Boroujeni N, Bokaeian M, Saeidi S, Jalaladdini M, Bazi S. Antimicrobial activity of Cyminum cuminum against biofilm E. coli. Int Res J Appl Basic Sci. 2013;6(3):286-8.

  • 44.

    Hassannejad N, Bahador A, Rudbari NH, Modarressi MH, Parivar K. In vivo antibacterial activity of Zataria multiflora Boiss extract and its components, carvacrol, and thymol, against colistin-resistant Acinetobacter baumannii in a pneumonic BALB/c mouse model. J Cell Biochem. 2019;120(11):18640-9. [PubMed ID: 31338900]. https://doi.org/10.1002/jcb.28908.

  • 45.

    Poovendran P. Antimicrobial activity of Mirabilis Jalapa and Dichrotachys cinerea against biofilm and extended spectrum of beta lactamase (ESBL) producing uropathogenic Escherichia coli. Afr J Microbiol Res. 2011;5(22). https://doi.org/10.5897/ajmr11.116.

  • 46.

    Amirkaveei S, Behbahani BA. Antimicrobial effect of mangrove extract on Escherichia coli and Penicillium digitatum. International Conference on Food Engineering and Biotechnology. 2011. p. 185-8.

  • 47.

    Sahraei S, Azizi A. Evaluation of the effect of antimicrobial activity of ethanol extract of Calotropis procera in Extended Spectrum Beta-Lactamase Producing E. coli. Int J Adv Biol Biomed Res. 2014;2(3):764-8.

  • 48.

    Growther L, Sukritha K, Savitha N, Andrew NS. Antibacterial activity of Punica granatum peel extracts against Shiga toxin producing E. coli. Int J Life Sci Bt and Pharm Res. 2012;4:1-11.

  • 49.

    Voravuthikunchai SP, Limsuwan S. Medicinal plant extracts as anti-Escherichia coli O157:H7 agents and their effects on bacterial cell aggregation. J Food Prot. 2006;69(10):2336-41. [PubMed ID: 17066910]. https://doi.org/10.4315/0362-028x-69.10.2336.

  • 50.

    Trabelsi A, El Kaibi MA, Abbassi A, Horchani A, Chekir-Ghedira L, Ghedira K. Phytochemical Study and Antibacterial and Antibiotic Modulation Activity of Punica granatum (Pomegranate) Leaves. Scientifica (Cairo). 2020;2020:8271203. [PubMed ID: 32318311]. [PubMed Central ID: PMC7150692]. https://doi.org/10.1155/2020/8271203.

  • 51.

    Chukwuka KS, Ikheloa JO, Okonko IO, Moody JO, Mankinde TA. The antimicrobial activities of some medicinal plants on Escherichia coli as an agent of diarrhea in livestock. Adv Appl Sci Res. 2011;2(4):37-48.

  • 52.

    Dongarwar A, Nimbekar T, Parshuramkar T, Indurwade N. Preparation and Evaluation of Herbal Formulation Using Natural Extract. Chem Methodol. 2019;3(4):451-6.

  • 53.

    Asghar MA, Zahir E, Shahid SM, Khan MN, Asghar MA, Iqbal J, et al. Iron, copper and silver nanoparticles: Green synthesis using green and black tea leaves extracts and evaluation of antibacterial, antifungal and aflatoxin B1 adsorption activity. Lwt. 2018;90:98-107. https://doi.org/10.1016/j.lwt.2017.12.009.

  • 54.

    Ramadhan M, Sabarudin A, Safitri A. In Vitro Anti-microbial Activity of Hydroethanolic Extracts of Ruellia tuberosa L.: Eco-friendly Based-product Against Selected Pathogenic Bacteria. IOP Conference Series: Earth and Environmental Science. 2019.

  • 55.

    Sawhney R, Berry V, Kumar A. Inhibitory Activity of Rubia cordifolia plant extract against ESBL producing Urinary E. coli isolates. J Pharm Res. 2012;5(3):1328-30.

  • 56.

    Slusarenko AJ, Patel A, Portz D. Control of plant diseases by natural products: Allicin from garlic as a case study. Sustainable disease management in a European context. . Springer; 2008. p. 313-22. https://doi.org/10.1007/978-1-4020-8780-6_10.

  • 57.

    Rahimi V, Hekmatimoghaddam S, Jebali A, Khalili Sadrabad E, Akrami Mohajeri F. Chemical Composition and Antifungal Activity of Essential Oil of Zataria Multiflora. J Nutr Food Secur. 2019;4(1):1-6. https://doi.org/10.18502/jnfs.v4i1.394.

  • 58.

    Mitic V, Jovanovic O, Stankov-Jovanovic V, Zlatkovic B, Stojanovic G. Analysis of the essential oil of Teucrium polium ssp. capitatum from the Balkan Peninsula. Nat Prod Commun. 2012;7(1):83-6. [PubMed ID: 22428254].

  • 59.

    Daroui-Mokaddem H, Kabouche A, Bouacha M, Soumati B, El-Azzouny A, Bruneau C, et al. GC/MS analysis and antimicrobial activity of the essential oil of fresh leaves of Eucalytus globulus, and leaves and stems of Smyrnium olusatrum from Constantine (Algeria). Nat Prod Commun. 2010;5(10):1669-72. [PubMed ID: 21121270].

  • 60.

    Rana VS. Chemical composition of the essential oil of Cuminum cyminum L. seeds from Western India. J Med Plants By-Product. 2014;3(2):207-10.

  • 61.

    Mohammed SI, Vishwakarma KS, Maheshwari VL. Evaluation of Larvicidal Activity of Essential Oil from Leaves of Coccinia grandis against Three Mosquito Species. J Arthropod Borne Dis. 2017;11(2):226-35. [PubMed ID: 29062847]. [PubMed Central ID: PMC5641611].

  • 62.

    Olufunke MD, Kasali AA, Olusegun E. Constituents of theSpondias mombinLinn and the Comparison between its Fruit and Leaf essential oils. J Essent Oil Bearing Plants. 2003;6(3):148-52. https://doi.org/10.1080/0972-060x.2003.10643343.

  • 63.

    Sonibare MA, Ogunwande IA, Walker TM, Setzer WN, Soladoye MO, Essien E. Volatile Constituents of Ficus Exasperata Leaves. Nat Prod Commun. 2019;1(9). https://doi.org/10.1177/1934578x0600100912.

  • 64.

    Kouame BKFP, Toure D, Kablan L, Bedi G, Tea I, Robins R, et al. Chemical Constituents and Antibacterial Activity of Essential Oils from Flowers and Stems of Ageratum conyzoides from Ivory Coast. Records Nat Prod. 2018;12(2):160-8. https://doi.org/10.25135/rnp.22.17.06.040.

  • 65.

    Moronkola DO, Ogukwe C, Awokoya KN. Chemical compositions of leaf and stem essential oils of Calotropis procera Ait R. Br [Asclepiadaceae]. Der Chemi Sinica. 2011;2(2):255-60.

  • 66.

    Zin N, Rahimi W, Bakar NA. A Review of Quercus infectoria (Olivier) Galls as a Resource for Anti-parasitic Agents: In Vitro and In Vivo Studies. Malays J Med Sci. 2019;26(6):19-34. [PubMed ID: 31908584]. [PubMed Central ID: PMC6939732]. https://doi.org/10.21315/mjms2019.26.6.3.

  • 67.

    Sukumaran S, Kiruba S, Mahesh M, Nisha SR, Miller PZ, Ben CP, et al. Phytochemical constituents and antibacterial efficacy of the flowers of Peltophorum pterocarpum (DC.) Baker ex Heyne. Asian Pac J Trop Biomed. 2011;4(9):735-8. https://doi.org/10.1016/s1995-7645(11)60183-1.

  • 68.

    Adewuyi AM, Akangbe YT, Animasaun DA, Durodola FA, Bello OB. Terminalia avicennioides as a potential candidate for pharmaceutical industry: a review. Res J Pharm Biol Chem Sci. 2015;6(2):748-54.

  • 69.

    Muhaisen HMH. Chemical constituents from the bark of Lannea acida rich (anacardiaceae). Scholars Res Lib. 2013;5(5):88-96.

  • 70.

    Joshi RK. Chemical Composition, In Vitro Antimicrobial and Antioxidant Activities of the Essential Oils of Ocimum Gratissimum, O. Sanctum and their Major Constituents. Indian J Pharm Sci. 2013;75(4):457-62. [PubMed ID: 24302801]. [PubMed Central ID: PMC3831728]. https://doi.org/10.4103/0250-474X.119834.

  • 71.

    Akhtar M, Ali M, Mir SR, Singh O. New anthraquinones from Rubia cordifolia roots. Indian J Chem. 1945;45B(8).